Naringenin attenuates CCl4-induced hepatic inflammation by the activation of an Nrf2-mediated pathway in rats

Clinical and Experimental Pharmacology and Physiology

Volumn 41, Issue 6, 2014, Pages 416-422

  Esmaeili, Mohammad Ali ^a   Alilou, Mostafa ^a  

^a SHAHID BEHESHTI UNIVERSITY   (Iran)

Author keywords

Carbon tetrachloride; Hepatotoxicity; Inflammation; Naringenin

Indexed keywords

ALKALINE PHOSPHATASE; AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CARBON TETRACHLORIDE; GLUTATHIONE; GLUTATHIONE TRANSFERASE ALPHA; HEME OXYGENASE; INDUCIBLE NITRIC OXIDE SYNTHASE; LACTATE DEHYDROGENASE; LIVER ENZYME; MESSENGER RNA; NARINGENIN; PROSTAGLANDIN SYNTHASE; SILYMARIN; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; FLAVANONE DERIVATIVE;

AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HISTOPATHOLOGY; LIPID PEROXIDATION; LIVER INJURY; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; ANIMAL; CHEMICAL STRUCTURE; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; DRUG-INDUCED LIVER INJURY; GENE EXPRESSION REGULATION; GENETICS; INFLAMMATION; METABOLISM; SIGNAL TRANSDUCTION; TOXICITY;

ANIMALS; CARBON TETRACHLORIDE; DRUG-INDUCED LIVER INJURY; FLAVANONES; GENE EXPRESSION REGULATION; INFLAMMATION; MOLECULAR STRUCTURE; NF-E2-RELATED FACTOR 2; RATS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SILYMARIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84901242029     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/1440-1681.12230     Document Type: Article

References (34)

1. Akindele AJ, Ezenwanebe KO, Anunobi CC, Adeyemi OO. Hepatoprotective and in vivo antioxidant effects of Byrsocarpus coccineus Schum. and Thonn (Connaraceae). J. Ethnopharmacol. 2010; 129: 46-52.
2. Williams AT, Burk RF. Carbon tetrachloride hepatotoxicity: An example of free radical-mediated injury. Semin. Liver Dis. 1990; 10: 279-84.
3. Aruoma OI. Nutrition and health aspects of free radicals and antioxidants. Food Chem. Toxicol. 1994; 32: 671-83.
4. Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol. 1978; 52: 302-10.
5. Esterbauer H, Schaur J, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal malonaldehyde and related aldehydes. Free Radic. Biol. Med. 1991; 11: 81-128.
6. Fan J, Zeng M, Li J. Correlation between hepatic fat, lipid peroxidation and hepatic fibrosis in rats chronically fed with ethanol and/or high fat diet. Zhonghua Nei Ke Za Zhi 1997; 12: 808-11.
7. Fang F, Tang Y, Gao Z, Xu Q. A novel regulatory mechanism of naringenin through inhibition of T lymphocyte function in contact hypersensitivity suppression. Biochem. Biophys. Res. Commun. 2010; 397: 163-9.
8. Farombi EO, Shrotriya S, Na HK, Kim SH, Surh YJ. Curcumin attenuates dimethylnitrosamine-induced liver injury in rats through Nrf2-mediated induction of heme oxygenase-1. Food Chem. Toxicol. 2008; 46: 1279-87.
9. Ganapathy E, Peramaiyan R, Rajasekaran D, Venkataraman M, Dhanapal S. Modulatory effect of naringenin on N-methyl-N′-nitro-N-nitrosoguanidineand saturated sodium chloride-induced gastric carcinogenesis in male wistar rats. Clin. Exp. Pharmacol. Physiol. 2008; 35: 1190-6.
10. Goldwasser J, Cohen PY, Lin W et al. Naringenin inhibits the assembly and longterm production of infectious hepatitis C virus particles through a PPAR mediated mechanism. J. Hepatol. 2011; 55: 963-71.
11. Griffith OW. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 1980; 106: 207-12.
12. Hayes JD, Ellis EM, Neal GE, Harrison DJ, Manson MM. Cellular response to cancer chemopreventive agents: Contribution of the antioxidant responsive element to the adaptive response to oxidative and chemical stress. Biochem. Soc. Symp. 1999; 64: 141-68.
13. Huang Q, Zhang S, Zheng L, He M, Huang R, Lin X. Hepatoprotective effects of total saponins isolated from Taraphochlamy saffinis against carbon tetra chloride induced liver injury in rats. Food Chem. Toxicol. 2012; 50: 713-8.
14. Itoh K, Chiba T, Takahashi S et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 1997; 236: 313-22.
15. Jia N, Liu X, Wen J et al. A proteomic method for analysis of CYP450s protein expression changes in carbon tetrachloride induced male rat liver microsomes. Toxicology 2007; 237: 1-11.
16. Leonardi T, Vanamala J, Taddeo SS et al. Apigenin and naringenin suppress colon carcinogenesis through the aberrant crypt stage in azoxymethane-treated rats. Exp. Biol. Med. (Maywood) 2010; 235: 710-7.
17. Manibusan MK, Odin M, Eastmond DA. Postulated carbon tetrachloride mode of action: A review. J. Environ. Sci. Health C. Environ. Carcinog. Ecotoxicol. Rev. 2007; 25: 185-209.
18. Pietta PG. Flavonoids as antioxidants. J. Nat. Prod. 2000; 63: 1035-42.
19. Lee MH, Yoon S, Moon JO. The flavonoid naringenin inhibits dimethylnitrosamine-induced liver damage in rats. Biol. Pharm. Bull. 2004; 27: 72-6.
20. Qin L, Jin L, Lu L et al. Naringenin reduces lung metastasis in a breast cancer resection model. Protein Cell 2006; 2: 507-16.
21. Ribeiro IA, Rocha J, Sepodes B, Mota-Filipe H, Ribeiro MH. Effect of naringin enzymatic hydrolysis towards naringenin on the anti-inflammatory activity of both compounds. J. Mol. Catal. B Enzyme 2008; 52: 13-8.
22. Rushmore TH, Morton MR, Pickett CB. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem. 1991; 266: 11632-9.
23. Sabarinathan D, Mahalakshmi P, Vanisree AJ. Naringenin promote apoptosis in cerebrally implanted C6 glioma cells. Mol. Cell. Biochem. 2010; 345: 215-22.
24. Slater TF. Free-radical mechanisms in tissue injury. Biochem. J. 1984; 222: 1-15.
25. Soromou LW, Zhang Z, Li R et al. Regulation of inflammatory cytokines in lipopolysaccharide-stimulated RAW 264.7 murine macrophage by 7-O-methyl-naringenin. Molecules 2012; 17: 3574-85.
26. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione. Applications to mammalian blood and other tissues. Anal. Biochem. 1964; 27: 502-22.
27. Tsukamoto H, Rippe R, Niemela O, Lin M. Roles of oxidative stress in activation of Kupffer and Ito cells in liver fibrogenesis. J. Gastroenterol. Hepatol. 1995; 10: 50-3.
28. Weber LW, Boll M, Stampfl A. Hepatotoxicity and mechanism of action of haloalkanes: Carbon tetrachloride as a toxicological model. Crit. Rev. Toxicol. 2003; 33: 105-36.
29. Aleksunes LM, Manautou JE. Emerging role of Nrf2 in protecting against hepatic and gastrointestinal disease. Toxicol. Pathol. 2007; 35: 459-73.
30. Moi P, Chan K, Asunis I, Cao A, Kan YW. Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc. Natl Acad. Sci. USA 1994; 91: 9926-30.
31. Nahmias Y, Goldwasser J, Casali M et al. Apolipoprotein B dependent hepatitis C virus secretion is inhibited by the grapefruit flavonoid naringenin. Hepatology 2008; 47: 1437-45.
32. Ortiz-Andrade RR, Sanchez-Salgado JC, Navarrete-Vazquez G et al. Antidiabetic and toxicological evaluations of naringenin in normoglycaemic and NIDDM rat models and its implications on extra-pancreatic glucose regulation. Diabetes Obes. Metab. 2008; 10: 1097-104.
33. Ozturk IC, Ozturk F, Gul M, Ates B, Cetin A. Protective effects of ascorbic acid on hepatotoxicity and oxidative stress caused by carbon tetrachloride in the liver of Wistar rats. Cell Biochem. Funct. 2009; 27: 309-15.
34. Pari L, Gnanasoundari M. Impact of naringenin on oxytetracycline-mediated oxidative damage in kidney of rats. Ren. Fail. 2006; 28: 599-605.